Abstract
It is now acknowledged that bacteria from gut microbiota deeply interact with their host by altering many physiological traits. Such interplay is likely to consequently affect stress tolerance. Here, we compared cold and heat tolerance of Drosophila melanogaster flies with undisrupted (control (Co)) versus disrupted gut microbiota (dechorionated eggs (De)). The disrupting treatment strongly reduced bacterial load in flies’ guts, though 16S sequencing analysis did not evidence strong diversity changes in the remaining bacterial community. Both chill coma recovery and acute cold survival were repeatedly lower in De than in Co flies under our experimental conditions. However, heat tolerance was not consistently affected by gut disruption. Our results suggest that microbiota-related effects on the host can alter ecologically relevant traits such as thermal tolerance.
References
Brummel T, Ching A, Seroude L, Simon AF, Benzer S (2004) Drosophila lifespan enhancement by exogenous bacteria. Proc Natl Acad Sci U S A 101:12974–12979. https://doi.org/10.1073/pnas.0405207101
Clark RI, Salazar A, Yamada R, Fitz-Gibbon S, Morselli M, Alcaraz J, Rana A, Rera M, Pellegrini M, Ja WW, Walker DW (2015) Distinct shifts in microbiota composition during Drosophila aging impair intestinal function and drive mortality. Cell Rep 12:1656–1667. https://doi.org/10.1016/j.celrep.2015.08.004
Colinet H, Renault D (2012) Metabolic effects of CO2 anaesthesia in Drosophila melanogaster. Biol Lett 8:1050–1054. https://doi.org/10.1098/rsbl.2012.0601
Colinet H, Larvor V, Bical R, Renault D (2013) Dietary sugars affect cold tolerance of Drosophila melanogaster. Metabolomics 9:608–622. https://doi.org/10.1007/s11306-012-0471-z
Engel P, Moran NA (2013) The gut microbiota of insects – diversity in structure and function. FEMS Microbiol Rev 37:699–735. https://doi.org/10.1111/1574-6976.12025
Jiménez Padilla Y (2016) Effects of gut-associated yeasts on Drosophila melanogaster performance. Electron Thesis Diss Repos
Koyle ML, Veloz M, Judd AM, Wong ACN, Newell PD, Douglas AE, Chaston JM (2016) Rearing the fruit fly Drosophila melanogaster under axenic and gnotobiotic conditions. J Vis Exp e54219–e54219. https://doi.org/10.3791/54219
Liu H, Dicksved J, Lundh T, Lindberg JE (2014) Heat shock proteins: intestinal gatekeepers that are influenced by dietary components and the gut microbiota. Pathogens 3:187–210. https://doi.org/10.3390/pathogens3010187
MacMillan HA, Yerushalmi GY, Jonusaite S et al (2017) Thermal acclimation mitigates cold-induced paracellular leak from the Drosophila gut. Sci Rep 7:8807. https://doi.org/10.1038/s41598-017-08926-7
Matos RC, Schwarzer M, Gervais H, Courtin P, Joncour P, Gillet B, Ma D, Bulteau AL, Martino ME, Hughes S, Chapot-Chartier MP, Leulier F (2017) D-Alanylation of teichoic acids contributes to Lactobacillus plantarum-mediated Drosophila growth during chronic undernutrition. Nat Microbiol 2:1635–1647. https://doi.org/10.1038/s41564-017-0038-x
McMurdie PJ, Holmes S (2013) phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One 8:e61217. https://doi.org/10.1371/journal.pone.0061217
Moghadam NN, Thorshauge PM, Kristensen TN, de Jonge N, Bahrndorff S, Kjeldal H, Nielsen JL (2017) Strong responses of Drosophila melanogaster microbiota to developmental temperature. Fly (Austin) 12:1–12. https://doi.org/10.1080/19336934.2017.1394558
Overend G, Luo Y, Henderson L, Douglas AE, Davies SA, Dow JAT (2016) Molecular mechanism and functional significance of acid generation in the Drosophila midgut. Sci Rep 6. https://doi.org/10.1038/srep27242
Overgaard J, MacMillan HA (2017) The integrative physiology of insect chill tolerance. Annu Rev Physiol 79:187–208. https://doi.org/10.1146/annurev-physiol-022516-034142
R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
Ridley EV, Wong AC-N, Westmiller S, Douglas AE (2012) Impact of the resident microbiota on the nutritional phenotype of Drosophila melanogaster. PLoS One 7:e36765. https://doi.org/10.1371/journal.pone.0036765
Ridley EV, Wong ACN, Douglas AE (2013) Microbe-dependent and nonspecific effects of procedures to eliminate the resident microbiota from Drosophila melanogaster. Appl Environ Microbiol 79:3209–3214. https://doi.org/10.1128/AEM.00206-13
Russell JA, Moran NA (2006) Costs and benefits of symbiont infection in aphids: variation among symbionts and across temperatures. Proc R Soc Lond B Biol Sci 273:603–610. https://doi.org/10.1098/rspb.2005.3348
Ryu J-H, Kim S-H, Lee H-Y, Bai JY, Nam YD, Bae JW, Lee DG, Shin SC, Ha EM, Lee WJ (2008) Innate immune homeostasis by the homeobox gene caudal and commensal-gut mutualism in Drosophila. Science 319:777–782. https://doi.org/10.1126/science.1149357
Schou MF, Mouridsen MB, Sørensen JG, Loeschcke V (2017) Linear reaction norms of thermal limits in Drosophila: predictable plasticity in cold but not in heat tolerance. Funct Ecol 31:934–945. https://doi.org/10.1111/1365-2435.12782
Shin SC, Kim S-H, You H, Kim B, Kim AC, Lee KA, Yoon JH, Ryu JH, Lee WJ (2011) Drosophila microbiome modulates host developmental and metabolic homeostasis via insulin signaling. Science 334:670–674. https://doi.org/10.1126/science.1212782
Soen Y (2014) Environmental disruption of host–microbe co-adaptation as a potential driving force in evolution. Front Genet 5. https://doi.org/10.3389/fgene.2014.00168
Staubach F, Baines JF, Künzel S, Bik EM, Petrov DA (2013) Host species and environmental effects on bacterial communities associated with Drosophila in the laboratory and in the natural environment. PLoS One 8:e70749. https://doi.org/10.1371/journal.pone.0070749
Teets NM, Denlinger DL (2013) Physiological mechanisms of seasonal and rapid cold-hardening in insects. Physiol Entomol 38:105–116. https://doi.org/10.1111/phen.12019
Wong AC-N, Chaston JM, Douglas AE (2013) The inconstant gut microbiota of Drosophila species revealed by 16S rRNA gene analysis. ISME J 7:1922–1932. https://doi.org/10.1038/ismej.2013.86
Wong AC-N, Dobson AJ, Douglas AE (2014) Gut microbiota dictates the metabolic response of Drosophila to diet. J Exp Biol 217:1894–1901. https://doi.org/10.1242/jeb.101725
Yamada R, Deshpande SA, Bruce KD, Mak EM, Ja WW (2015) Microbes promote amino acid harvest to rescue undernutrition in Drosophila. Cell Rep 10:865–872. https://doi.org/10.1016/j.celrep.2015.01.018
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Authors thank the GeT-PLaGe plateform for Miseq sequencing.
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Henry, Y., Colinet, H. Microbiota disruption leads to reduced cold tolerance in Drosophila flies. Sci Nat 105, 59 (2018). https://doi.org/10.1007/s00114-018-1584-7
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DOI: https://doi.org/10.1007/s00114-018-1584-7